Frequency-independent characteristics of high-frequency oscillations in epileptic and non-epileptic regions

OBJECTIVE The purpose of the presented study is to determine whether there are frequency-independent high-frequency oscillation (HFO) parameters which may differ in epileptic and non-epileptic regions. METHODS We studied 31 consecutive patients with medically intractable focal (temporal and extratemporal) epilepsies who were examined by either intracerebral or subdural electrodes. Automated detection was used to detect HFO. The characteristics (rate, amplitude, and duration) of HFO were statistically compared within three groups: the seizure onset zone (SOZ), the irritative zone (IZ), and areas outside the IZ and SOZ (nonSOZ/nonIZ). RESULTS In all patients, fast ripples (FR) and ripples (R) were significantly more frequent and shorter in the SOZ than in the nonSOZ/nonIZ region. In the group of patients with favorable surgical outcomes, the relative amplitude of FR was higher in the SOZ than in the IZ and nonIZ/nonSOZ regions; in patients with poor outcomes, the results were reversed. The relative amplitude of R was significantly higher in the SOZ, with no difference between patients with poor and favorable surgical outcomes. CONCLUSIONS FR are more frequent, shorter, and have higher relative amplitudes in the SOZ area than in other regions. The study suggests a worse prognosis in patients with higher amplitudes of FR outside the SOZ. SIGNIFICANCE Various HFO parameters, especially of FR, differ in epileptic and non-epileptic regions. The amplitude and duration may be as important as the frequency band and rate of HFO in marking the seizure onset region or the epileptogenic area and may provide additional information on epileptogenicity.

[1]  Andreas Schulze-Bonhage,et al.  Temporal and spatial characteristics of high frequency oscillations as a new biomarker in epilepsy , 2015, Epilepsia.

[2]  D. Louis Collins,et al.  High‐frequency oscillations, extent of surgical resection, and surgical outcome in drug‐resistant focal epilepsy , 2013, Epilepsia.

[3]  Michael X. Cohen,et al.  Intracranial EEG Correlates of Expectancy and Memory Formation in the Human Hippocampus and Nucleus Accumbens , 2010, Neuron.

[4]  Charles L. Wilson,et al.  Local Generation of Fast Ripples in Epileptic Brain , 2002, The Journal of Neuroscience.

[5]  Gabriel Curio,et al.  Somatotopic source arrangement of 600 Hz oscillatory magnetic fields at the human primary somatosensory hand cortex , 1997, Neuroscience Letters.

[6]  Jan Chrastina,et al.  Interictal high-frequency oscillations indicate seizure onset zone in patients with focal cortical dysplasia , 2010, Epilepsy Research.

[7]  Hellmuth Obrig,et al.  Stimulus-Induced and State-Dependent Sustained Gamma Activity Is Tightly Coupled to the Hemodynamic Response in Humans , 2009, The Journal of Neuroscience.

[8]  Premysl Jiruska,et al.  High-frequency activity in experimental and clinical epileptic foci , 2011, Epilepsy Research.

[9]  Hitten P. Zaveri,et al.  The spatial and signal characteristics of physiologic high frequency oscillations , 2014, Epilepsia.

[10]  Justin A. Blanco,et al.  Data mining neocortical high-frequency oscillations in epilepsy and controls. , 2011, Brain : a journal of neurology.

[11]  Pavel Jurák,et al.  Impact of cognitive stimulation on ripples within human epileptic and non-epileptic hippocampus , 2015, BMC Neuroscience.

[12]  Jean Gotman,et al.  Interictal high-frequency oscillations (100-500 Hz) in the intracerebral EEG of epileptic patients. , 2007, Brain : a journal of neurology.

[13]  Jean Gotman,et al.  Interictal high frequency oscillations (HFOs) in patients with focal epilepsy and normal MRI , 2012, Clinical Neurophysiology.

[14]  J. Gotman,et al.  High frequency oscillations in intracranial EEGs mark epileptogenicity rather than lesion type. , 2009, Brain : a journal of neurology.

[15]  Shuang Wang,et al.  Ripple classification helps to localize the seizure‐onset zone in neocortical epilepsy , 2013, Epilepsia.

[16]  B. Brinkmann,et al.  Pathological and physiological high-frequency oscillations in focal human epilepsy. , 2013, Journal of neurophysiology.

[17]  J. Gotman,et al.  High‐frequency electroencephalographic oscillations correlate with outcome of epilepsy surgery , 2010, Annals of neurology.

[18]  Jeffery A. Hall,et al.  Interictal high‐frequency oscillations (80–500 Hz) are an indicator of seizure onset areas independent of spikes in the human epileptic brain , 2008, Epilepsia.

[19]  J. Gotman,et al.  Effect of sleep stage on interictal high‐frequency oscillations recorded from depth macroelectrodes in patients with focal epilepsy , 2009, Epilepsia.

[20]  J. Martinerie,et al.  Mapping interictal oscillations greater than 200 Hz recorded with intracranial macroelectrodes in human epilepsy. , 2010, Brain : a journal of neurology.

[21]  E. Halgren,et al.  High-frequency neural activity and human cognition: Past, present and possible future of intracranial EEG research , 2012, Progress in Neurobiology.

[22]  B. Litt,et al.  High-frequency oscillations in human temporal lobe: simultaneous microwire and clinical macroelectrode recordings. , 2008, Brain : a journal of neurology.

[23]  Charles L. Wilson,et al.  Quantitative analysis of high-frequency oscillations (80-500 Hz) recorded in human epileptic hippocampus and entorhinal cortex. , 2002, Journal of neurophysiology.

[24]  Charles L. Wilson,et al.  Hippocampal and Entorhinal Cortex High‐Frequency Oscillations (100–500 Hz) in Human Epileptic Brain and in Kainic Acid‐Treated Rats with Chronic Seizures , 1999, Epilepsia.

[25]  Keiko Usui,et al.  Significance of Very‐High‐Frequency Oscillations (Over 1,000Hz) in Epilepsy , 2015, Annals of neurology.

[26]  G. Buzsáki,et al.  High-Frequency Oscillations in the Output Networks of the Hippocampal–Entorhinal Axis of the Freely Behaving Rat , 1996, The Journal of Neuroscience.

[27]  Charles L. Wilson,et al.  High‐frequency Oscillations after Status Epilepticus: Epileptogenesis and Seizure Genesis , 2004, Epilepsia.

[28]  Jean Gotman,et al.  Improving the identification of High Frequency Oscillations , 2009, Clinical Neurophysiology.

[29]  Jerome Engel,et al.  High-frequency oscillations in epileptic brain , 2010, Current opinion in neurology.

[30]  I. Módy,et al.  High-frequency oscillations : What is normal and what is not ? , 2008 .

[31]  Jeremy R. Manning,et al.  Broadband Shifts in Local Field Potential Power Spectra Are Correlated with Single-Neuron Spiking in Humans , 2009, The Journal of Neuroscience.

[32]  Masaaki Nishida,et al.  Cortical glucose metabolism positively correlates with gamma-oscillations in nonlesional focal epilepsy , 2008, NeuroImage.

[33]  G. Buzsáki,et al.  High-frequency network oscillation in the hippocampus. , 1992, Science.

[34]  J. Jefferys,et al.  High‐frequency oscillations as a new biomarker in epilepsy , 2012, Annals of neurology.

[35]  Charles L. Wilson,et al.  High‐frequency oscillations in human brain , 1999, Hippocampus.

[36]  Jean Gotman,et al.  The identification of distinct high-frequency oscillations during spikes delineates the seizure onset zone better than high-frequency spectral power changes , 2016, Clinical Neurophysiology.

[37]  G Curio,et al.  Linking 600-Hz “Spikelike” EEG/MEG Wavelets (“&sfgr;-Bursts”) to Cellular Substrates: Concepts and Caveats , 2000, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[38]  G. Mathern,et al.  Removing interictal fast ripples on electrocorticography linked with seizure freedom in children , 2010, Neurology.

[39]  Eishi Asano,et al.  Spontaneous and visually driven high‐frequency oscillations in the occipital cortex: Intracranial recording in epileptic patients , 2012, Human brain mapping.

[40]  W. Singer,et al.  Hemodynamic Signals Correlate Tightly with Synchronized Gamma Oscillations , 2005, Science.

[41]  B. Litt,et al.  High-frequency oscillations and seizure generation in neocortical epilepsy. , 2004, Brain : a journal of neurology.

[42]  Jerome Engel,et al.  Voltage Depth Profiles of High‐frequency Oscillations after Kainic Acid‐induced Status Epilepticus , 2007, Epilepsia.

[43]  Ayako Ochi,et al.  Focal resection of fast ripples on extraoperative intracranial EEG improves seizure outcome in pediatric epilepsy , 2011, Epilepsia.

[44]  H. Lüders,et al.  Presurgical evaluation of epilepsy. , 2001, Brain : a journal of neurology.